BLOGS

Around 1870, a tiny Chinese insect turned up in farm fields around the city of San Jose, California. The creature would inject a syringe-like mouthpart into a plant and suck up the juices. It grew a plate-like shield that covered its entire body, out from which new insects would eventually emerge. The San Jose scale, as the insect came to be known, spread quickly through the United States and Canada, leaving ravaged orchards in its path. “There is perhaps no insect capable of causing greater damage to fruit interests in the United States, or perhaps the world, than the San Jose scale,” one entomologist declared.

Farmers searched for pesticides that could stop the San Jose scale. In the nineteenth century, they had a fearsome arsenal of poisons for killing weeds and insects. In the ancient empire of Sumer 4500 years ago, farmers put sulfur on their crops. The Romans used pitch and grease. Europeans learned to extract chemicals from plants. In 1807, chemists isolated pyrethrum from an Armenian daisy. To stop the San Jose scale, they tried whale oil. They tried kerosene and water. One of the best treatments they found was a mix of lime and sulfur. After a few weeks of spraying, the San Jose scale would disappear.

By 1900, however, the lime-sulfur cure was failing. Here and there, the San Jose scale returned to its former abundance. An entomologist named A. L. Melander found some San Jose scales living happily under a thick crust of dried lime-sulfur spray. So Melander embarked on a widespread experiment, testing out sulfur-lime on orchards across Washington State. He found that in some orchards, the pesticide wiped out the insects completely. In other orchards, as many as 13 percent of the scales survived. But those surviving scales could be killed off with kerosene.

Melander wondered why some populations of scales were becoming able to resist pesticides. Could the sulfur-lime spray trigger a change in their biology, the way manual labor triggers the growth of callouses on our hands? Melander doubted it. After all, ten generations of scales lived and died between sprayings. The resistance must be hereditary, he reasoned. He sometimes would find families of scales still alive amidst a crowd of dead insects.

This was a radical idea at the time. Biologists had only recently rediscovered Mendel’s laws of heredity. They talked about genes being passed down from one generation to the next, yet they didn’t know what genes were made of yet. But they did recognize that genes could spontaneously change–mutate–and in so doing alter traits permanently.

“The sporadic occurrence of naturally immune individual scales finds a parallel in recent work on heredity of protozoa and bacteria,” Melander declared in 1914. “Mutants less or not susceptible to certain toxins have been repeatedly found in cultures and from them have been produced immune strains.”

In the short term, Melander suggested that farmers switch to fuel oil to fight scales, but he warned that they would eventually become resistant to fuel oil as well. In fact, the best way to keep the scales from becoming entirely resistant to pesticides was, paradoxically, to do a bad job of applying those herbicides. By allowing some susceptible scales to survive, farmers would keep their susceptible genes in the scale population. “Thus we may make the strange assertion that the more faulty the spraying this year the easier it will be to control the scale the next year,” Melander predicted.

Melander is one of evolution’s unsung heroes. Nearly a century ago, he demonstrated how natural selection could happen very quickly, and have a direct effect on people’s lives. Unfortunately, his great insight appears to have fallen on deaf ears. For the next few decades, farmers and chemists gave little thought to the possibility that insects or weeds would evolve resistance. Gradually, however, it became clear that every time they tried a new chemical, the target of that chemical began to evolve resistance to it. And the more they sprayed a chemical, the faster the resistance evolved.

As chemicals failed, chemists searched for new ones. The search got harder and harder. Making the task more challenging was the fact that these chemicals can be extremely nasty not just to weeds or pests, but to beneficial insects, birds, and even humans. But in 1970 a scientist at the Monsanto Corporation found a chemical that seemed to hold out great hope–glyphosate, also known as Roundup.

Glyphosate kills weeds by blocking the construction of amino acids that are essential for the survival of plants. It attacks enzymes that only plants use, with the result that it’s harmless to people, insects, and other animals. And unlike other herbicides that wind up in ground water, glyphosate stays where it’s sprayed, degrading within weeks.

Roundup went on the market in 1974. In 1986, scientists engineered plants to be resistant to glyphosate, by inserting genes from bacteria that could produce amino acids even after a plant was sprayed with herbicides. In the 1990s Monsanto and other companies began to sell glyphosate-resistant corn, cotton, sugar beets, and many other crops. The crops proved hugely popular. Instead of applying a lot of different herbicides, farmers found they could hit their fields with a modest amount of glyphosate alone, which wiped out weeds without harming their crops. Studies indicate that farmers who used the transgenic crops used fewer herbicides than those who grew regular plants —77% less in Mexico, for example—while getting a significantly higher yield from their fields.

For a while, it seemed as if glyphosate would avoid Melander’s iron rule. Monsanto scientists ran tests that showed no evidence of resistance. Glyphosate seemed to strike at such an essential part of plant biology that plants could not evolve a defense. But after glyphosate-resistant crops had a few years to grow, farmers began to notice horseweed and morning glory and other weeds encroaching once more into their fields. Farmers in Georgia had to cut down fields of cotton rather than harvest them because of infestations of Palmer amaranth.

In today’s New York Times William Neuman and Andrew Pollack have a sobering article about just how bad things have gotten for farmers who use glyphosate over the past decade. They begin with the story of one Tennessee farmer, Eddie Anderson:

For 15 years, Eddie Anderson, a farmer, has been a strict adherent of no-till agriculture, an environmentally friendly technique that all but eliminates plowing to curb erosion and the harmful runoff of fertilizers and pesticides.

But not this year.

On a recent afternoon here, Mr. Anderson watched as tractors crisscrossed a rolling field — plowing and mixing herbicides into the soil to kill weeds where soybeans will soon be planted.

“What we’re talking about here is Darwinian evolution in fast-forward,” Mike Owen, a weed scientist at Iowa State University, told Neuman and Pollack.

Neuman and Pollack left the story of this fast-forward evolution at that–but it’s actually a fascinating tale. A century ago, Melander could only study natural selection by observing which insects lived and died. Today, scientists can pop the lid off the genetic toolbox that insects and weeds use to resist chemicals that were once thought irresistible. Stephen Powles, a scientist at the University of Western Australia, has been studying the evolution of Roundup resistance for some years now, and he’s co-authored a new review that surveys what we know now about it.

What’s striking is how many different ways weeds have found to overcome the chemical. Scientists had thought that Roundup was invincible in part because the enzyme it attacks is pretty much the same in all plants. That uniformity suggests that plants can’t tolerate mutations to it; mutations must change its shape so that it doesn’t work and the plant dies. But it turns out that many populations of ryegrass and goosegrass have independently stumbled across one mutation that can change a single amino acid in the enzyme. The plant can still survive with this altered enzyme. And Roundup has a hard time attacking it thanks to its different shape.

Another way weeds fight off Roundup is through sheer numbers. Earlier this year an international team of scientists reported their discovery of how Palmer amaranth resists glyphosate. The plants make the ordinary, vulnerable form of the enzyme. But the scientists discovered that they have many extra copies of the gene for the enzyme–up to 160 extra copies, in fact. All those extra genes make extra copies of the enzyme. While the glyphosate may knock out some of the enzymes in the Palmer amaranth, the plants make so many more enzymes that they can go on growing.

It’s also possible for weeds to evolve resistance to Roundup without any change whatsoever to the enzyme Roundup attacks. When farmers spread Roundup on plants, the chemical spreads swiftly from the leaves all the way down the stems to the roots. This fast, widespread movement helps make Roundup so deadly. It turns out that some species of horseweed and other weeds have evolved a way to block the spread. Scientists don’t yet know how they manage this. It’s possible that cells in the leaves suck the Roundup in through their membranes and then tuck it away in safe little chambers where they can’t cause harm. However they do it, the weeds can continue to grow with their normal enzymes.

What makes the evolution of Roundup resistance all the more dangerous is how it doesn’t respect species barriers. Scientists have found evidence that once one species evolves resistance, it can pass on those resistance genes to other species. They just interbreed, producing hybrids that can then breed with the vulnerable parent species.

In a recent interview, Powles predicted that the Roundup resistance catastophe is just going to get worse, not just in the United States but everywhere where Roundup is used intensively. It’s not a hopeless situation, however. Farmers may be able to slow the spread of resistance by mixing up the kinds of seeds they use, even by fostering vulernable weeds in the way Melander suggested. Resistance is a manageable problem–once you recognize the problem and its evolutionary roots.

In fact, the best way to keep the scales from becoming entirely resistant to pesticides was, paradoxically, to do a bad job of applying those herbicides. By allowing some susceptible scales to survive, farmers would keep their susceptible genes in the scale population.

Oh wow. In hte 1990s Mike Shaw developed some models of fungicide resistance that showed the same thing. I hadn’t realized the idea was so old.

“Scientists have found evidence that once one species evolves resistance, it can pass on those resistance genes to other species. They just interbreed, producing hybrids that can breed with the vulnerable parent species.”

Very interesting, I don’t doubt it for a second but it contradicts what we have long been told what defines a species, a barrier keeping it from succesfully breeding with other species. I’m not a scientist but it always struck me that that it is possible evolution itself has tricks we have not yet discovered, some kind of adaptability in times of stress.

Hey Jim Bob
Would that be round up ready marijuana? The story almost writes itself, two disgruntled Monsanto employees take a vacation to Amsterdamn, make a half serious business pitch to a marijuana seed seller, who takes them totally seriously and puts them to work. Two years later a new product hits the market and marijuana becomes legal because it’s unstoppable.

It’s interesting that what was always considered the rate-limiting step in the evolution of resistance to a pesticide/antibiotic (a mutation that confers resistance) can occur easily and often (especially in really large populations). Because these resistance mutations are so common, we need to devise better strategies to prevent their spread — possibly by taking advantage of sensitive individuals out-competing the resistant ones.

Dave (3), the species barrier is a general rule. Biology doesn’t always like fitting into our human-made classifications. E.g. dogs, wolves, coyotes are all different species but they can interbreed. Plants especially can do this plus do other weird things like having multiple sets of the same genes (polyploidy), or transferring sets of genes between species. There is only one steadfast rule in biology–all rules have exceptions, including this one.

In regards to your second statement about evolution still having tricks, I fully agree. I think we ain’t seen nothing yet, to borrow an old phrase. What I found slightly puzzling was that scientists felt Roundup was ‘invincible’? It seems it would be just a matter of time before “life will find a way”–maybe those scientists should have watched Jurassic Park?

Sounds like a title of a book Carl Zimmer will write ten years from now when the science of genetics has grown expotentially and the wild speculations of today are the confirmed hypothesis of tommorrow. There is reason for wild optimism in the continued growth of genetics. It happened in computers and DNA is just a biological counterpart to the lines of computer code.

Carl, a heartfelt thank you from a huge fan of science for assembling such a top flight team of bloggers under the Discover banner. It was very forward thinking of you and it will pay off big time, you make sure and tell the bottom line boys over there exactly that.

I am puzzled by this:
“Thus we may make the strange assertion that the more faulty the spraying this year the easier it will be to control the scale the next year,” Melander predicted.
Powles and Yu say in their article:
“However, selection at lower herbicide dose (most plants killed but some survivors) selects for all possible resistance-endowing genes, both weak and strong. Especially in cross-pollinated species this can allow the rapid accumulation of resistance genes.”

I too am puzzled by Melander’s assertion that faulty spraying is key to avoiding resistance.

My understanding was that the way to avoid resistance was the opposite, very diligent spraying. You have to avoid survivors and exposure to less than lethal concentrations of the control agent.

Once you have conditions that produce survivors, the survivors are the ones who got less exposure and/or genetically based resistance. Those survivors get together, breed, and pass along any advantageous genes. Another round of spraying, more survivors, some of whom are likely more resistant than their parents. A populator stressor, producing conditions that favour the resistant members of the population.

Eventually you may get a population that is mostly or entirely resistant to your control agent. Darwinian selection, right there.